Born in Washington, North Carolina, Hamilton displayed an early interest in performing during his days at Washington High School just before America's entry into World War II. Bad hearing kept him from enlisting, so he moved to New York City as a 19-year-old to find a career on stage.[citation needed]
In an early role, he performed on stage with Henry Fonda in the classic wartime story Mister Roberts as a replacement for David Wayne, playing Ensign Pulver. In 1960, he was onstage again with Fonda in Critic's Choice; Howard Taubman of The New York Times called him "properly obnoxious as the director". Hamilton was teamed once more with Fonda in 1968 for the drama film The Boston Strangler.
His best known performance is as Larry Vaughn, the obdurate mayor of Amity, in the Steven Spielberg thriller Jaws (1975). Hamilton reprised the role in the sequel, Jaws 2 in 1978. He was approached to reprise his role in Jaws: The Revenge, but died in 1986 aged 63 . Other notable big-screen appearances include the critically acclaimed 1959 film Anatomy of a Murder with James Stewart, in which he played the bartender Al Pacquette, who gives testimony in the murder of Barney Quill. He also worked with Stewart in The Spirit of St. Louis (1957) and The FBI Story (1959).

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